brain research 1564 (2014) 1–8

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Research Report

Effects of exposure to an extremely low frequency electromagnetic field on hippocampal long-term potentiation in rat Alireza Komakin, Afshin Khalili, Iraj Salehi, Siamak Shahidi, Abdolrahman Sarihi Neurophysiology Research Center, Hamadan University of Medical Sciences, Hamadan, Iran

art i cle i nfo

ab st rac t

Article history:

Modern lifestyle exposes nearly all humans to electromagnetic fields, particularly to extremely

Accepted 28 March 2014

low frequency electromagnetic fields (ELF-EMFs). Prolonged exposure to ELF-EMFs induces

Available online 12 April 2014

persistent changes in neuronal activity. However, the modulation of synaptic efficiency by ELF-

Keywords:

EMFs in vivo is still unclear. In the present study, we investigated whether ELF-EMFs can change

Extremely low-frequency magnetic

induction of long-term potentiation (LTP) and paired-pulse ratio (PPR) in the rat hippocampal

field

area. Twenty-nine adult male Wistar rats were divided into 3 groups (ELF-EMF exposed, sham

Long-term potentiation

and control groups). The ELF-EMF group was exposed to a magnetic field for 90 consecutive days

Rat

(2 h/day). ELF-EMFs were produced by a circular coil (50 Hz, 100 micro Tesla). The sham-exposed

Hippocampus

controls were placed in an identical chamber with no electromagnetic field. After this period, rats were deeply anesthetized with urethane (2.0 mg/kg) and then a bipolar stimulating and recording electrode was implanted into the perforant pathway (PP) and dentate gyrus (DG), respectively. LTP in hippocampal area was induced by high-frequency stimulation (HFS). Prolonged exposure to ELF-EMFs increased LTP induction. There was a significant difference in the slope of EPSP and amplitude of PS between the ELF-EMF group and other groups. In conclusion, our data suggest that exposure to ELF-EMFs produces a marked change in the synaptic plasticity generated in synapses of the PP-DG. No significant difference in PPR of ELFEMF group before and after HFS suggests a postsynaptic expression site of LTP. & 2014 Elsevier B.V. All rights reserved.

1.

Introduction

The widespread use of electricity increases the potential sources of radiation resulting in continuous and or intermittent

exposure of living beings to extremely low frequency electromagnetic fields (ELF-EMFs) (Boland et al., 2002). Whether ELFEMF induces health hazards has been disputed since the issue first became prominent (Marino and Becker, 1978) and the

n Correspondence to: Department of Physiology, School of Medicine, Hamadan University of Medical Sciences, Shahid Fahmideh Street, P.O. Box 65178/518, Hamadan, Iran. Fax: þ98 811 8380131. E-mail addresses: [email protected], [email protected], [email protected] (A. Komaki). URL: http://umsha.ac.ir (A. Komaki).

http://dx.doi.org/10.1016/j.brainres.2014.03.041 0006-8993/& 2014 Elsevier B.V. All rights reserved.

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brain research 1564 (2014) 1–8

results in this respect are equivocal. Therefore, more experimental works relevant to the identification of possible mechanisms are needed (Mostafa et al., 2002; Vázquez-García et al., 2004; Rajkovic et al., 2005; Wolf et al., 2005; Varró et al., 2009; Modolo et al., 2013; Salehi et al., 2013; Salunke et al., 2013). Several epidemiological studies reported an association between ELF-EMF exposure and several disorders, including neurodegenerative disorders (Sobel et al., 1996) and cancers (Tynes et al., 1992; Ahlbom et al., 2000). Moreover, experiments performed in order to study the cellular effect of EMFs have shown that EMFs can induce cell proliferation (Katsir and Parola, 1998), alteration of DNA integrity (Koana et al., 1997), variations of intracellular calcium concentration (Yost and Liburdy, 1992; Wieraszko, 2000) and perturbations of the central nervous system inducing behavioral disturbances in animals (Lai, 1996; Lai and Carino, 1999; Boland et al., 2002). Over the past decades, continued evidence has demonstrated that ELF-EMFs produce effects on cognition, nervous system function and brain activity (Sienkiewicz et al., 2005). However, relatively limited studies have been done on the effects of ELF-EMFs on the nervous system function (Liu et al., 2008). A number of studies have suggested that ELF-EMFs may interact with learning and memory processes (Kavaliers et al., 1993; Lai, 1996; Lai and Carino, 1999; Mostafa et al., 2002; Vázquez-García et al., 2004). Up to now, there have been existed a few studies related to the effects of magnetic field exposure on synaptic plasticity in the rat hippocampus (Ahmed and Wieraszko, 2008, Balassa et al., 2013), a brain region found to be essential for memory storage and consolidation (Nadel, 1991; Eichenbaum, 1992; Ahmed and Wieraszko, 2008). However, the mechanisms by which the magnetic stimulation modulates synaptic efficiency remain unclear. Long-term potentiation (LTP), which is prominently expressed in the hippocampus, is currently considered as an important model for studying the mechanisms of persistent alteration in central nervous system synaptic efficiency, leading to learning and memory formation (Teyler and DiScenna, 1987; Bliss and Collingridge, 1993; Morgan and Teyler, 1999; Teyler et al., 2001; Bear and Linden, 2001; Morris et al., 2003). There are many mechanisms associated with LTP induction, including enhancement of transmitter release, the activation of AMPA and NMDA receptors, and changes in the number of synaptic-spine contacts and in the shape of the spine heads (Lee et al., 1980; Bekkers and Stevens, 1990; Bliss and Collingridge, 1993). The present study was conducted to evaluate the effect of a long-term ELF-EMFs (100 mT) on LTP and paired-pulse ratio (PPR). Magnetic fields around most household appliances and equipment typically do not exceed 150 mT. The aim of the present study was to determine whether long-term (3 months) exposure to ELF-EMF influences hippocampal synaptic plasticity in vivo; and if so, to identify the place underlying this effect. To address this question, we analyzed the paired-pulse ratio (PPR) of two responses evoked by two successive stimuli at given intervals. Any change in presynaptic sites is expected to accompany changes in PPR (Zucker, 1989; Jiang et al., 2004; Manita et al., 2007; Salazar-Weber and Smith, 2011; Komaki et al., 2013). PPR is the ratio of the second response amplitude to that of the first and has been used as a successful measure of vesicular release probability (Manita et al., 2007; Salazar-Weber and Smith, 2011).

Fig. 1 – The electromagnetic exposure system. The temporal homogeneity is defined by measuring the magnetic field strength at different times. The calculated magnetic field strength was 100 μT. The ELF-EMF-exposed group was exposed to ELF-EMFs in their home cages at the middle of the exposure system and the sham-exposed controls were placed in the system with no electromagnetic field.

2.

Results

2.1.

Measurement of evoked potentials

The evoked field potential in the DG has two components: Population Spike (PS); and field Excitatory Postsynaptic Potentials (fEPSP) (Fig. 2). PS and fEPSP responses were driven by bipolar stimuli (100–500 mA). During electrophysiological recordings, changes in PS amplitude and fEPSP slope were measured. The amplitude of the PS was measured from the peak of the first positive deflection of the evoked potential to the peak of the following negative potential. The fEPSP slope function was measured as the slope of the line connecting the start of the first positive deflection of the evoked potential with the peak of the second positive deflection of the evoked potential. The stimulation intensity was adjusted to evoke potentials, comprising 40% of the maximal population spike amplitude, defined by means of an input/output curve.

brain research 1564 (2014) 1–8

3

Paired-Pulse (20 ms) 1 mv 5 ms

Before HFS

Population Spikes Paired-Pulse (30 ms) Slope of fEPSP

After HFS Paired-Pulse (40 ms)

Fig. 2 – (A) Representative sample traces of field potential recorded in the PP-DG synapses prior to and 120 min after HFS induction. Arrows indicate population spikes. (B) A representative example of field potential evoked by paired-pulse stimulation at intervals of 20, 30 and 40 ms after the HFS application.

Control

200

Sham

control (13577% of pre-HFS baseline) and sham (12978% of pre-HFS baseline) groups. There was no significant difference of fEPSP slope between the control and Sham groups (p40.05). These results indicate that HFS directly applied to the perforant pathway-DG can enhance synaptic transmission, inducing LTP in the ELF-EMF group (16379% of pre-HFS baseline). This enhancement was significantly higher than that in the control and Sham groups (po0.01).

EPSP Slope (% of baseline)

ELF-EMF

180

160

140

120

100

2.3.

80 Base

5

30

60

120

Time (Min)

Fig. 3 – EPSP slope of three experimental groups in the DG granular cell synapses of the hippocampus. HFS stimulation is applied at the arrowhead, and a clear difference between the ELF-EMF group and other groups is seen in the EPSP slopes. The data represent (mean7SEM, % of baseline) for field Potential recording. *po0.05, **po0.01 significant difference (ELF-EMFs in comparison with control )

Fig. 4 demonstrates that the amplitude of PS (60 min after HFS) was 243712% of pre-HFS baseline in the control group (n¼ 10), 255713% of pre-HFS baseline in the sham group (n¼ 9), and 314718% of pre-HFS baseline in the ELF-EMF group (n ¼10). The amplitude of PS was significantly higher than that in the control and Sham groups (po0.01). Fig. 4 also demonstrates there was no significant difference of amplitude of PS LTP between the control and Sham groups (p40.05). These results indicated that chronic exposure to ELF-EMF increased both fEPSP slope and PS amplitude.

2.4. 2.2.

Effect of ELF-EMFs on the amplitude of PS

Effects of LTP induction on PPR of evoked potential

Effect of ELF-EMFs on the slope of EPSP

The effects of ELF-EMFs on the LTP of EPSP induced by highfrequency stimulation (HFS) in the PP to the DG area of the hippocampus in rats were examined. As shown in Fig. 3, the slopes of fEPSP were strongly enhanced, resulting in a significant amount of LTP (60 min after HFS) at PP-DG synapses in

In the next set of experiments, the ratios of the second amplitude to the first field potentials evoked by paired stimulation at intervals of 20, 30 and 40 ms were plotted for each group (Fig. 5). Paired-pulse stimulation affected all field potential components at intervals o200 ms. The largest changes occurred at intervals between 20–30 ms. No significant effects

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brain research 1564 (2014) 1–8

Control

380

Sham ELF-EMF

PS Amplitude (%)

330 280 230 180 130 80 Base

5

30

60

120

Time (Min)

Fig. 4 – Time-dependent changes in hippocampal responses to perforant path following HFS stimulation. HFS stimulation is applied at the arrowhead, and a clear difference between the ELF-EMF group and other groups is seen in the population spike. The data represent (mean7SEM, % of baseline) for field potential recording. *po0.05, **po0.01 significant difference (ELF-EMFs in comparison with control )

2

Control Before HFS

Control After HFS

Sham Before HFS

Sham After HFS

ELF-EMF Before HFS

ELF-EMF After HFS

1.8

Paired-pulse Ratio

1.6 1.4 1.2 1 0.8 0.6 0.4 0.2 0 20

30

40

Interpulse Interval (ms)

Fig. 5 – Paired-pulse ratio of evoked field potential was not changed by HFS. In the graph, ratios of the amplitude of the second to first field potentials evoked by paired stimulation at intervals of 20, 30 and 40 ms are plotted for all groups. Values obtained before and after the induction of LTP by HFS. All data are expressed as means7SEM. High Frequency Stimulation (HFS), extremely low frequency electromagnetic fields (ELF-EMFs).

of LTP induction on PPF were observed. In other words, the PPR of the evoked field potential was not changed by HFS (p40.05).

3.

Discussion

The main purpose of the present study is to investigate whether long-term exposure to ELF-EMFs can influence synaptic plasticity in rat hippocampal in vivo. The most remarkable observation in our study was that ELF-EMFs increased the development of LTP whereas it had no effect on PPR.

Along with the rapid increase in the applications of electric power and electrical facilities, exposures to ELFEMFs are significantly enhanced in both intensity and duration (Lacy-Hulbert et al., 1998). Most of the world's population is chronically exposed to electromagnetic fields of less than 0.1 mT (BioInitiative Report, 2012). The ELF-EMF is induced with the current flow and, therefore, cannot be shielded by common materials, making ELF-EMFs much harder to avoid (Liu et al., 2008). To explore the long-term effect of EMF exposure on synaptic plasticity,we compared the induction of LTP in DG of control and ELF-EMFs groups. There is one clear characteristic in our study in that the first ELF-EMF exposure (in vivo) was carried out on rats for three months followed by the induction of LTP by HFS. The first finding of this study was that exposure of adult rat to ELF-EMFs produces a marked increase in the induction of LTP generated in synapses of the PP-DG in vivo. The current descriptions of EMF effects on hippocampal neuronal plasticity in terms of LTP/LTD are sparse in the literature (Levkovitz and Segal, 2001; Wieraszko, 2004; Kim et al., 2006; Tokay et al., 2009; Prochnow et al., 2011; Balassa et al., 2013). The first indication of direct synaptic modulation by magnetic fields alone with long-lasting (30 min) magnetic stimulation was reported in 2004 (Wieraszko, 2004). In support of our findings, reports of enhanced short- and long-term synaptic facilitation in hippocampal slices and increased seizure susceptibility in neocortical slices were observed following whole-body exposure to ELF-EMFs (Varró et al., 2009). Several hypotheses have been advanced on the functional significance of the increased neuroplasticity related to hippocampal neurogenesis in the DG (Duman et al., 2000; Feng et al., 2001; Gould et al., 1999; Greenough et al., 1999; Jacobs et al., 2000; Cuccurazzu et al., 2010). One of the numerous stimuli known to modulate adult neurogenesis is electromagnetic field radiation (Arias-Carrión et al., 2004; Czéh et al., 2002). It has been shown that exposure to ELF-EMF significantly enhances the neuronal differentiation of cortical neural stem/progenitor cells (NSCs) in vitro, and this effect is mediated by the upregulation of Cav1-channel expression and activity (Piacentini et al., 2008). It is well established that the entry of Ca2þ ions through these channels can influence the transcription of certain classes of genes involved in cell survival and differentiation (Hardingham et al., 1998; Orrenius et al., 2003; West et al., 2001). In an alternative hypothesis, it has been concluded that Ca2þ ion dissociation from a low-affinity binding site is the electromagnetic fieldsensitive step (Pilla et al., 1999; Lagace et al., 2009). The existence of a causal link between ELF-EMF-enhanced neurogenesis and increased synaptic plasticity is supported by a number of experimental studies, which show that environmental, behavioral and pharmacological factors known to increase or decrease hippocampal adult neurogenesis have corresponding effects on DG LTP (Saxe et al., 2006; Wang et al., 2008; Zhao et al., 2006; Cuccurazzu et al., 2010). Another hypothesis of effects related to ELF-EMF is that it changes free radical levels in organisms. ELF-EMF converts free radicals into less active molecules and eliminates them (Genestra, 2007; Valko et al., 2007). There is a balance between production and elimination of free radicals – an imbalance can promote oxidative stress, eventually resulting in cell

brain research 1564 (2014) 1–8

destruction (Moore and Roberts, 1998; Ozdemir and Kargi, 2011). Also, indicated is the involvement of NMDA receptor in ELF-EMF and its effects on anxiety behavior in mice (Salunke et al., 2013). In the next set of experiments, to address the place of synaptic plasticity, we analyzed the paired-pulse ratio (PPR). Here, we found no significant differences before and after HFS in all groups, suggesting a postsynaptic expression site of LTP (Jiang et al., 2004; Manita et al., 2007; Salazar-Weber and Smith, 2011; Zucker, 1989; Tokay et al., 2009). Our present findings clearly show that synaptic plasticity, which is widely considered as a model of cellular learning, is improved by ELF-EMF exposure. Together, these data confirm that HFSinduced LTP is expressed postsynaptically. In conclusion, it can be said that ELF-EMFs may change the synaptic plasticity in rat DG and suggests a postsynaptic expression site of this neuronal plasticity. This is the first experiment to evaluate the effect of chronic exposure of ELFEMF on hippocampal synaptic plasticity in rat. Further studies on other regions related to learning and memory, such as cortex, are suggested for fully understanding of ELF-EMF effects on synaptic plasticity.

4.

Experimental Procedures

4.1.

Animals

Male Wistar albino rats (200 g) were obtained from the animal facilities of Razi Institute, Karaj, Iran. Prior to all experimental settings, animals were subjected to the same conditions: Rats were housed in groups of 5 animals per cage in a temperature-controlled room (22 1C72) under artificial illumination (12:12 light/dark cycle; lighted from 07:00 to 19:00). Water and food were given ad libitum. After one week of adaptation, subjects were randomly separated into ELF-EMFexposed, sham-exposed and control groups. The number of rats in each condition was: ELF-EMF-exposed (n¼ 10) shamexposed (n¼ 9) and control (n¼ 10). To test the influence of a magnetic field, the ELF-EMF-exposed group was exposed to a flux density of 100 μT and frequency of 50 Hz, 2 h/day for 3 months, from 10:00–12:00,. The sham-exposed subjects were placed in identical chamber with no electromagnetic field from 12:00–14:00. Control subjects were not exposed to the chamber. This study received permission from the Animal Care and Research Committee of Hamadan University of Medical Sciences, Hamadan, Iran.

4.2.

Electromagnetic exposure system

Exposure system and application of electromagnetic field in this study were described previously (Salehi et al., 2013). In brief, the exposure unit comprised of a solenoid coil with length of 2 m, radius of 20 cm and 1000 turns per meter (Fig. 1). The diameter of the copper wire was 2 mm. A 220 V and 50 Hz sinusoidal power frequency current was fed through the solenoid in the exposure system. An adjustable resistance circuit was connected to the power source to generate the electric field and, consequently, the magnetic field. The prepared circuit was able to generate an effective

5

magnetic field in the range of 0–2000 μT, with a sinusoidal wave of frequency of 50 Hz. The magnetic flux density was measured with a teslameter (Koshava 3: Wuntronic GmbH, Germany) and the density was adjusted by varying the coil current using an external resistance circuit (Mevissen et al., 1998; Salehi et al., 2013).

4.3.

Surgical method

Animals were food and water deprived for 1 h prior to surgery. The electrophysiological study was carried out one day after the last exposure session. The experimental groups were put in the magnetic field one after another with 2 days latency and the field potential recording was performed right after 3 months magnetic treatment which took 1 or 2 days for each group. For electrophysiological recording, the rats were anesthetized with Urethane (1.5 g/kg i.p., with supplemental injections as required) and stereotaxically implanted with two bipolar teflon-coated silver electrodes (125 μm diameter); a stimulating electrode in the perforant pathway (PP) (coordinates: AP = 6.8 mm, ML = 4.1 mm, DV = 3 mm, from skull surface), and a recording electrode in the dentate gyrus (DG) granule cell layer (coordinates: AP = 2.8 mm, ML = 1.8 mm, DV = 3 mm, from skull surface). Electrodes were placed according to the Paxinos and Watson atlas of the rat brain (Paxinos and Watson, 2005). The electrodes were lowered very slowly (0.2 mm/min) from the cortex to the hippocampus to minimize brain tissue trauma. Electrode positions were optimized to record maximal population spike (PS). The stimulating and recording sites in the hippocampus were confirmed histologically from brain sections. The electrophysiological responses depend on the exact location of electrodes. These electrophysiological findings confirm the histological observations which indicate the place of the stimulating electrodes were located in PP. For recording electrodes they were located in DG.

4.4.

Input–output current

Input–output current profiles were obtained by stimulating the PP to determine the optimal stimulus intensity for each subject (40% maximal population spike). Single 0.1 ms biphasic square wave pulses were delivered through constant current isolation units (A365 WPI, USA) at a frequency of 0.1 Hz. The field potential recordings were obtained in the granular cells of the DG following stimulation of the PP. Test stimuli were delivered to the PP every 10 s. Electrodes were positioned to elicit the maximum amplitude of PS and fEPSP. The slope of fEPSP was calculated as the amplitude change at 20–80% of the voltage difference between the start of the waveform and the fEPSP amplitude at the onset of PS. After a steady-state baseline response was ensured, taken after 40 min, LTP was induced using a HFS protocol of 400 Hz (10 bursts of 20 stimuli, 0.2 ms stimulus duration, 10 s interburst interval) at a stimulus intensity that evoked a PS amplitude and a fEPSP slope of approximately 80% of the maximum response (Fig. 2). Both fEPSP and PS were recorded at 5, 30, 60 and 120 min after the HFS to determine any changes in the synaptic response of DG neurons. For each time-point, 10

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consecutive evoked responses were averaged at 10 s stimulus intervals (Taube and Schwartzkroin, 1988, Karimi et al., 2013). For stimulations, the parameters of the stimuli were defined in Biochart software (Science Beam, Iran) and were sent via a data acquisition board linked to a constant current isolator unit (A365 WPI) prior to delivery to the PP through the stimulus electrodes. The induced field potential response from the DG was passed through a preamplifier, and was amplified (1000  ) (Differential amplifier DAM 80 WPI, USA), and filtered (band pass 1 Hz to 3 kHz). This response was digitized at a sampling rate of 10 kHz, and was observable on a computer (and an oscilloscope). It was saved in a file to facilitate later offline analysis. Data were statistically analyzed by repeated measures ANOVA tests followed by Tukey's test. Values of po0.05 were considered to be significant.

Acknowledgments The authors wish to thank Lori Sims at Brooklyn College of City University of New York (CUNY) for revising the paper as a native English speaker and for her excellent comments. This research was supported by a Grant from the Neurophysiology Research Center, Hamadan University of Medical Sciences, Hamadan, Iran. The authors would like to express their gratitude to the staff of the Neurophysiology Research Center for helping them carry out this project.

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Effects of exposure to an extremely low frequency electromagnetic field on hippocampal long-term potentiation in rat.

Modern lifestyle exposes nearly all humans to electromagnetic fields, particularly to extremely low frequency electromagnetic fields (ELF-EMFs). Prolo...
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